Interaction of acetylcholinesterase with neurexin-1β regulates glutamatergic synaptic stability in hippocampal neurons

Mol Brain. 2014 Mar 5:7:15. doi: 10.1186/1756-6606-7-15.

Abstract

Background: Excess expression of acetylcholinesterase (AChE) in the cortex and hippocampus causes a decrease in the number of glutamatergic synapses and alters the expression of neurexin and neuroligin, trans-synaptic proteins that control synaptic stability. The molecular sequence and three-dimensional structure of AChE are homologous to the corresponding aspects of the ectodomain of neuroligin. This study investigated whether excess AChE interacts physically with neurexin to destabilize glutamatergic synapses.

Results: The results showed that AChE clusters colocalized with neurexin assemblies in the neurites of hippocampal neurons and that AChE co-immunoprecipitated with neurexin from the lysate of these neurons. Moreover, when expressed in human embryonic kidney 293 cells, N-glycosylated AChE co-immunoprecipitated with non-O-glycosylated neurexin-1β, with N-glycosylation of the AChE being required for this co-precipitation to occur. Increasing extracellular AChE decreased the association of neurexin with neuroligin and inhibited neuroligin-induced synaptogenesis. The number and activity of excitatory synapses in cultured hippocampal neurons were reduced by extracellular catalytically inactive AChE.

Conclusions: Excessive glycosylated AChE could competitively disrupt a subset of the neurexin-neuroligin junctions consequently impairing the integrity of glutamatergic synapses. This might serve a molecular mechanism of excessive AChE induced neurodegeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholinesterase / metabolism*
  • Animals
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Cell Membrane / metabolism
  • Glutamates / metabolism*
  • Glycosylation
  • HEK293 Cells
  • Hippocampus / cytology*
  • Humans
  • Immunoprecipitation
  • Ligands
  • Models, Biological
  • Nerve Tissue Proteins / metabolism*
  • Neurons / metabolism*
  • Protein Binding
  • RNA Splicing
  • Rats
  • Rats, Wistar
  • Synapses / metabolism*

Substances

  • Cell Adhesion Molecules, Neuronal
  • Glutamates
  • Ligands
  • Nerve Tissue Proteins
  • neurexin Ibeta
  • Acetylcholinesterase